Serum IL-23 levels reflect a myeloid inflammatory signature and predict the response to apremilast in patients with psoriatic arthritis

Front Immunol. 2024 Dec 4:15:1455134. doi: 10.3389/fimmu.2024.1455134. eCollection 2024.

Abstract

Background: The phosphodiesterase 4 (PDE4) inhibitor apremilast downregulates the production of IL-23 and other pro-inflammatory cytokines involved in the pathogenesis of psoriatic arthritis (PsA).

Aim: To investigate the effects of apremilast on the production of cytokines by peripheral blood monocyte-derived macrophages, innate-like lymphocyte cells (ILCs), mucosal-associated invariant T (MAIT) cells, γδ T cells, natural killer (NK) cells, and NKT-like cells from patients with PsA manifesting different clinical responses to the treatment.

Methods: Peripheral blood samples were obtained from patients with PsA at baseline and after 1 and 4 months of apremilast therapy (n = 23) and 20 controls with osteoarthritis. Cytokine expression in peripheral blood monocyte-derived macrophages and ILCs/MAIT/γδT/NK/NKT-like cells was tested by RT-PCR and FACS analyses, respectively; cytokine levels in culture supernatants and sera were analyzed by ELISA.

Results: PsA monocyte-derived macrophages exhibited higher expressions of IL-23, IL-1β, and TNF-α, compared with OA controls, more profoundly in patients responding to apremilast. There were 17/23 (74%) PsA patients who were classified as responders to apremilast at 4 months, and a baseline serum IL-23 >1.4 pg/mL was associated with the responder status (AUCROC 0.79; sensitivity 100%, specificity 68%). Of note, apremilast led to a significantly reduced expression of IL-23 in peripheral blood monocyte-derived macrophages; IL-17 in ILC1 and in T cells of responder patients; IFN-γ in γδ T lymphocytes.

Conclusion: An enhanced myeloid inflammatory signature characterizes PsA monocyte-derived macrophages, and serum IL-23 levels represent candidate biomarkers for PsA response to apremilast.

Keywords: cytokines; immunology; innate lymphocyte; macrophages; precision medicine; spondyloarthritis (including psoriatic arthritis).

MeSH terms

  • Adult
  • Aged
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology
  • Anti-Inflammatory Agents, Non-Steroidal / therapeutic use
  • Arthritis, Psoriatic* / blood
  • Arthritis, Psoriatic* / drug therapy
  • Arthritis, Psoriatic* / immunology
  • Biomarkers / blood
  • Cytokines / blood
  • Female
  • Humans
  • Interleukin-23* / blood
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Middle Aged
  • Phosphodiesterase 4 Inhibitors / pharmacology
  • Phosphodiesterase 4 Inhibitors / therapeutic use
  • Thalidomide* / analogs & derivatives
  • Thalidomide* / pharmacology
  • Thalidomide* / therapeutic use
  • Treatment Outcome

Substances

  • apremilast
  • Thalidomide
  • Interleukin-23
  • Biomarkers
  • Anti-Inflammatory Agents, Non-Steroidal
  • Phosphodiesterase 4 Inhibitors
  • Cytokines

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. Financial support for this research was unconditionally provided by Amgen as part of the grant Amgen 20207131.